Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae)

Abstract

Background Polyploidy has played a major role in angiosperm evolution. Previous studies have examined polyploid phenotypes in comparison to their extant progenitors, but not in context of predicted progenitor phenotypes at allopolyploid origin. In addition, differences in the trends of polyploid versus diploid evolution have not been investigated. We use ancestral character-state reconstructions to estimate progenitor phenotype at allopolyploid origin to determine patterns of polyploid evolution leading to morphology of the extant species. We also compare trends in diploid versus allopolyploid evolution to determine if polyploidy modifies floral evolutionary patterns. Results Predicting the ancestral phenotype of a nascent allopolyploid from reconstructions of diploid phenotypes at the time of polyploid formation generates different phenotype predictions than when extant diploid phenotypes are used, the outcome of which can alter conclusions about polyploid evolution; however, most analyses yield the same results. Using ancestral reconstructions of diploid floral phenotypes indicate that young polyploids evolve shorter, wider corolla tubes, but older polyploids and diploids do not show any detectable evolutionary trends. Lability of the traits examined (floral shape, corolla tube length, and corolla tube width) differs across young and older polyploids and diploids. Corolla length is more evolutionarily labile in older polyploids and diploids. Polyploids do not display unique suites of floral characters based on both morphological and color traits, but some suites of characters may be evolving together and seem to have arisen multiple times within Nicotiana , perhaps due to the influence of pollinators. Conclusions Young polyploids display different trends in floral evolution (shorter, wider corolla tubes, which may result in more generalist pollination) than older polyploids and diploids, suggesting that patterns of divergence are impacted by the early consequences of allopolyploidy, perhaps arising from genomic shock and/or subsequent genome stabilization associated with diploidization. Convergent evolution in floral morphology and color in Nicotiana can be consistent with pollinator preferences, suggesting that pollinators may have shaped floral evolution in Nicotiana . Electronic supplementary material The online version of this article (10.1186/s12870-019-1771-5) contains supplementary material, which is available to authorized users.

Differential Gene Expression with an Emphasis on Floral Organ Size Differences in Natural and Synthetic Polyploids of Nicotiana tabacum (Solanaceae)

“…Intriguingly, synthetic allopolyploids have significantly wider cells than naturally occurring allopolyploids that arose approximately 0.6 million years ago [87]. This suggests that increased cell size in polyploids may attenuate over time [71], which correlates with our results that young polyploids tend to have wider corolla tubes than expected while older polyploids do not [90]. However, this attenuation of cell size in natural polyploids does not seem to be due solely to reduction of genome size following polyploidy because the natural N. tabacum genome has only downsized 3.7% compared to the expected sum of its progenitors [148].…”

“…This intermediate cell size is consistent with the fact that tube width in section Repandae is intermediate between progenitor morphology, as expected [91]. The potential reversion to a diploid-like cell size over time may explain why older polyploids do not display the same trends in corolla tube width evolution as young polyploids [90]. Again, this reversion to a diploid-like cell size does not seem to be correlated to genome size because two of the section Repandae species examined have genome sizes that have increased following polyploidy based on the sum of their diploid progenitors [148].…”

“…Young allopolyploids tend to evolve shorter and wider corolla tubes than expected based on the mean of the morphology of their progenitors, which may allow for a greater variety of pollinator types to access the nectar rewards of these flowers [90,91]. Cell width, cell number, and ploidy positively influence corolla tube circumference, and polyploids have significantly wider cells than diploids, with either the same number of cells or fewer (Figure 2).…”

“…Nicotiana is an excellent system to study polyploidy because approximately half of the species are allotetraploids which arose via six polyploidy events [84][85][86][87][88][89][90]. Polyploids of different ages, along with available synthetic lines created from the same progenitor species as natural polyploids, allow for investigation into the consequences of immediate, short-term, and long-term polyploid evolution.…”

“…In addition, Nicotiana displays wide variation in corolla tube length and width [91]. Young Nicotiana polyploids (<1 million years old (myo)) tend to evolve shorter and wider corolla tubes than what would be expected based on the intermediate values of their diploid progenitors, whereas diploids and older polyploids (> 1 myo) do not show any trends in corolla tube size evolution [90].…”